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Is Sexual Selection Driving Diversification of the Bioluminescent

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Is Sexual Selection Driving Diversification of the Bioluminescent Molecular Ecology (2011) 20, 2818–2834 doi: 10.1111/j.1365-294X.2011.05112.x Is sexual selection driving diversification of the bioluminescent ponyfishes (Teleostei: Leiognathidae)? PROSANTA CHAKRABARTY,* MATTHEW P. DAVIS,* W. LEO SMITH,† ZACHARY H. BALDWIN‡§ and JOHN S. SPARKS‡ *Museum of Natural Science (Ichthyology Section), Louisiana State University, 119 Foster Hall, Baton Rouge, LA 70803, USA, †Department of Zoology (Ichthyology), The Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, USA, ‡Division of Vertebrate Zoology (Ichthyology), American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA, §Richard Gilder Graduate School, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA Abstract Sexual selection may facilitate genetic isolation among populations and result in increased rates of diversification. As a mechanism driving diversification, sexual selection has been invoked and upheld in numerous empirical studies across disparate taxa, including birds, plants and spiders. In this study, we investigate the potential impact of sexual selection on the tempo and mode of ponyfish evolution. Ponyfishes (Leiognathidae) are bioluminescent marine fishes that exhibit sexually dimorphic features of their unique light-organ system (LOS). Although sexual selection is widely considered to be the driving force behind ponyfish speciation, this hypothesis has never been formally tested. Given that some leiognathid species have a sexually dimorphic LOS, whereas others do not, this family provides an excellent system within which to study the potential role of sexual selection in diversification and morphological differentiation. In this study, we estimate the phylogenetic relationships and divergence times for Leiognathidae, investigate the tempo and mode of ponyfish diversification, and explore morphological shape disparity among leiognathid clades. We recover strong support for a monophyletic Leiognathidae and estimate that all major ponyfish lineages evolved during the Paleogene. Our studies of ponyfish diversification demonstrate that there is no conclusive evidence that sexually dimorphic clades are significantly more species rich than nonsexually dimorphic lineages and that evidence is lacking to support any significant diversification rate increases within ponyfishes. Further, we detected a lineage-through-time signal indicating that ponyfishes have continuously diversified through time, which is in contrast to many recent diversification studies that identify lineage-through-time patterns that support mechanisms of density-dependent speciation. Additionally, there is no evidence of sexual selection hindering morphological diversity, as sexually dimorphic taxa are shown to be more disparate in overall shape morphology than nonsexually dimorphic taxa. Our results suggest that if sexual selection is occurring in ponyfish evolution, it is likely acting only as a genetic isolating mechanism that has allowed ponyfishes to continuously diversify over time, with no overall impact on increases in diversification rate or morphological disparity. Keywords: bioluminescence, disparity, diversification, leiognathids, sexual selection Received 24 September 2010; revision received 2 March 2011; accepted 14 March 2011 Correspondence: Prosanta Chakrabarty, Fax: 225-578-3075; E-mail: [email protected] Ó 2011 Blackwell Publishing Ltd TESTING FOR SEXUAL SELECTION IN PONYFISHES 2819 organs (by volume) than similarly sized conspecific Introduction females, but typically exhibit characteristic translucent Sexual selection may influence the tempo and mode of patches on their flank, gular, buccal, nuchal and ⁄ or evolution by facilitating genetic isolation among popu- opercular regions (Sparks et al. 2005; Chakrabarty & lations (Andersson 1994). In this study, we investigate Sparks 2007). These sexually dimorphic LOS traits allow whether sexual selection caused increased rates of males to both utilize and emit bacterially generated diversification in a family of bioluminescent fishes that luminescence in unique ways not available to females, utilize photic displays during courtship behaviour. Sex- which lack these anatomical specializations. Given that ual selection has been conjectured to be the driving these male-specific LOS traits would appear to make force behind speciation in leiognathids (ponyfishes) males more conspicuous to predators, it has been because of their highly variable and strongly sexually- hypothesized that the LOS is a target of sexual selection dimorphic luminescent system, but this hypothesis has and that these selective pressures could lead to genetic remained untested until now. In theory, if sexual selec- isolation and taxonomic diversification (Sparks et al. tion is occurring within Leiognathidae, it may lead to 2005). accelerated rates of diversification and produce repro- Sexual selection has previously been hypothesized to ductive isolation independent of environmental factors be an important isolating factor in the diversification of (Panhuis et al. 2001). There have been many compara- ponyfishes (Sparks et al. 2005) given that (i) leiognath- tive studies of the potential effects of sexual selection ids are externally conservative in morphology and are on speciation in various taxa that corroborate these the- often found in mixed confamilial species assemblages oretical signals (e.g. Mitra et al. 1996; Møller & Cuervo whose members lack conspicuous external sexually 1998; Hodges & Arnold 1995; Masta & Maddison 2002). dimorphic features (exclusive of translucent patches) Leiognathids are a common and widespread family and physiognomy (McFall-Ngai & Dunlap 1983; Sparks of shallow-water Indo-Pacific marine fishes that are et al. 2005), (ii) leiognathids are, in general, found in diagnosed by the presence of a unique light-organ sys- great abundance throughout their range with few obvi- tem (LOS). The circumesophageal light organ houses ous geographical isolating barriers and (iii) ponyfishes symbiotic bioluminescent bacteria (Photobacterium), have pelagic larvae that are theoretically capable of dis- which produce light that the host fish co-opts for preda- persing over great distances via ocean currents (Trnski tor avoidance via ventral counter-illumination, distress & Leis 2000). The LOS therefore represents the only displays, and for courtship signalling (Harvey 1921; character complex of sexually dimorphic anatomical Hastings 1971; McFall-Ngai & Dunlap 1984; Woodland traits (apart from anatomical differences related to sex et al. 2002; Sasaki et al. 2003). The LOS is comprised of itself) known in the family. Herein, we investigate a multilobed circumesophageal light organ, a silvery, whether rates of diversification and morphological dif- guanine-lined gas bladder, and translucent regions of ferentiation in body shape are influenced by potential the gas bladder, head and ⁄ or trunk that are frequently sexual-selective pressures acting on the LOS. species-specific in morphology (Sparks et al. 2005; Cha- The main objectives of this work are to: (i) reconstruct krabarty & Sparks 2007; Chakrabarty et al. 2011). Bacte- a comprehensive phylogeny for Leiognathidae, (ii) esti- rial luminescence is transmitted from the light organ mate divergence times for all major ponyfish lineages, into the reflective, guanine-lined gas bladder via a chro- (iii) examine the tempo and mode of ponyfish diversifi- matophore studded light organ ‘window’, which along cation and (iv) investigate morphological disparity in with muscular shutters on the light organ and corre- both body plan and the LOS. We analyse a greatly sponding chromatophore studded translucent head and expanded taxonomic sampling of ponyfishes relative to flank regions, controls the emission of light into the previous phylogenetic studies (Ikejima et al. 2004; environment (McFall-Ngai & Dunlap 1983; Sparks et al. Sparks & Dunlap 2004; Sparks et al. 2005) to resolve the 2005). The orientation, shape and pigmentation of the relationships of ponyfishes in a Bayesian framework, translucent external patches differ among ponyfish while simultaneously estimating lineage divergence clades, and it can be inferred that the intensity, flashing times via the inclusion of leiognathid and other acanth- pattern, and possibly wavelength of emitted light varies omorph fossils. Results of this analysis are then used as interspecifically based on morphological differences a framework for addressing questions regarding pony- associated with the LOS. fish diversification rates and morphological disparity In addition to species-specific LOS variation, most lei- that we outline below. ognathid species are sexually dimorphic with regard to To examine whether sexual selection acting on the light organ volume and shape (McFall-Ngai & Dunlap LOS has affected the tempo and mode of ponyfish 1984; Sparks et al. 2005). In ponyfishes with sexually diversification, we address three major questions. Is dimorphic LOSs, males not only have larger light there greater taxonomic richness in sexually dimorphic Ó 2011 Blackwell Publishing Ltd 2820 P. CHAKRABARTY ET AL. clades vs. the nondimorphic lineages? Are increased body shape). In contrast, the nonsexually dimorphic rates of diversification associated with sexually dimor- LOS lineages may exhibit greater morphological dispar- phic clades? Are lineage accumulation patterns consis- ity in external body form because of chance, given that tent with density-dependent speciation or continuous allopatric
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